IRF4 Transcription-Factor-Dependent CD103+CD11b+ Dendritic Cells Drive Mucosal T Helper 17 Cell Differentiation

Immunity

Volumn 38, Issue 5, 2013, Pages 958-969

  Persson, EmmaK ^a   Uronen Hansson, Heli ^a   Semmrich, Monika ^a   Rivollier, Aymeric ^a   Hägerbrand, Karin ^a   Marsal, Jan ^b   Gudjonsson, Sigurdur ^b   Håkansson, Ulf ^b   Reizis, Boris ^c   Kotarsky, Knut ^a   Agace, William W ^a,d  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

^c NewYork Presbyterian Hospital   (United States)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; CD135 ANTIGEN; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 17; INTERLEUKIN 6;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD103+CD11B+ DENDRITIC CELL; CELL COUNT; CELL DIFFERENTIATION; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINE CELL; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PHENOTYPE; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TH17 CELL;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD11B; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; DENDRITIC CELLS; HUMANS; INTEGRIN ALPHA CHAINS; INTERFERON REGULATORY FACTORS; INTERLEUKIN-17; INTESTINAL MUCOSA; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SEQUENCE DELETION; TH17 CELLS;

EID: 84878167904     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.03.009     Document Type: Article

References (68)

1. Abraham C., Medzhitov R. Interactions between the host innateimmune system and microbes in inflammatory bowel disease. Gastroenterology 2011, 140:1729-1737.
2. Aliberti J., Schulz O., Pennington D.J., Tsujimura H., Reis e Sousa C., Ozato K., Sher A. Essential role for ICSBP in the invivo development of murine CD8alpha+ dendritic cells. Blood 2003, 101:305-310.
3. Bachem A., Guttler S., Hartung E., Ebstein F., Schaefer M., Tannert A., Salama A., Movassaghi K., Opitz C., Mages H.W., et al. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J.Exp. Med. 2010, 207:1273-1281.
4. Bain C.C., Scott C.L., Uronen-Hansson H., Gudjonsson S., Jansson O., Grip O., Guilliams M., Malissen B., Agace W.W., Mowat A.McI. Local differentiation of resident and inflammatory macrophages from monocytes in human and mouse intestine. Mucosal Immunol. 2012, 6:498-510.
5. Bajana S., Roach K., Turner S., Paul J., Kovats S. IRF4 promotes cutaneous dendritic cell migration to lymph nodes during homeostasis and inflammation. J.Immunol. 2012, 189:3368-3377.
6. Beitnes A.C., Raki M., Lundin K.E., Jahnsen J., Sollid L.M., Jahnsen F.L. Density of CD163+ CD11c+ dendritic cells increases and CD103+ dendritic cells decreases in the coeliac lesion. Scand. J. Immunol. 2011, 74:186-194.
7. Bogunovic M., Ginhoux F., Helft J., Shang L., Hashimoto D., Greter M., Liu K., Jakubzick C., Ingersoll M.A., Leboeuf M., et al. Origin of the lamina propria dendritic cell network. Immunity 2009, 31:513-525.
8. Caton M.L., Smith-Raska M.R., Reizis B. Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. J.Exp. Med. 2007, 204:1653-1664.
9. Cerovic V., Houston S.A., Scott C.L., Aumeunier A., Yrlid U., Mowat A.M., Milling S.W. Intestinal CD103(-) dendritic cells migrate in lymph and prime effector Tcells. Mucosal Immunol. 2012, 6:104-113.
10. Coombes J.L., Powrie F. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 2008, 8:435-446.
11. Coombes J.L., Siddiqui K.R., Arancibia-Carcamo C.V., Hall J., Sun C.M., Belkaid Y., Powrie F. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory Tcells via a TGF-beta and retinoic acid-dependent mechanism. J.Exp. Med. 2007, 204:1757-1764.
12. Crozat K., Guiton R., Contreras V., Feuillet V., Dutertre C.A., Ventre E., Vu Manh T.P., Baranek T., Storset A.K., Marvel J., et al. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha+ dendritic cells. J.Exp. Med. 2010, 207:1283-1292.
13. Denning T.L., Norris B.A., Medina-Contreras O., Manicassamy S., Geem D., Madan R., Karp C.L., Pulendran B. Functional specializations of intestinal dendritic cell and macrophage subsets that control Th17 and regulatory Tcell responses are dependent on the Tcell/APC ratio, source of mouse strain, and regional localization. J.Immunol. 2011, 187:733-747.
14. Dudziak D., Kamphorst A.O., Heidkamp G.F., Buchholz V.R., Trumpfheller C., Yamazaki S., Cheong C., Liu K., Lee H.W., Park C.G., et al. Differential antigen processing by dendritic cell subsets invivo. Science 2007, 315:107-111.
15. Edelson B.T., Kc W., Juang R., Kohyama M., Benoit L.A., Klekotka P.A., Moon C., Albring J.C., Ise W., Michael D.G., et al. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J.Exp. Med. 2010, 207:823-836.
16. Fujimoto K., Karuppuchamy T., Takemura N., Shimohigoshi M., Machida T., Haseda Y., Aoshi T., Ishii K.J., Akira S., Uematsu S. A new subset of CD103+CD8alpha+ dendritic cells in the small intestine expresses TLR3, TLR7, and TLR9 and induces Th1 response and CTL activity. J.Immunol. 2011, 186:6287-6295.
17. Ginhoux F., Liu K., Helft J., Bogunovic M., Greter M., Hashimoto D., Price J., Yin N., Bromberg J., Lira S.A., et al. The origin and development of nonlymphoid tissue CD103+ DCs. J.Exp. Med. 2009, 206:3115-3130.
18. Goto Y., Kiyono H. Epithelial barrier: an interface for the cross-communication between gut flora and immune system. Immunol. Rev. 2012, 245:147-163.
19. Hammerschmidt S.I., Ahrendt M., Bode U., Wahl B., Kremmer E., Forster R., Pabst O. Stromal mesenteric lymph node cells are essential for the generation of gut-homing Tcells invivo. J.Exp. Med. 2008, 205:2483-2490.
20. Helft J., Ginhoux F., Bogunovic M., Merad M. Origin and functional heterogeneity of non-lymphoid tissue dendritic cells in mice. Immunol. Rev. 2010, 234:55-75.
21. Hildner K., Edelson B.T., Purtha W.E., Diamond M., Matsushita H., Kohyama M., Calderon B., Schraml B.U., Unanue E.R., Diamond M.S., et al. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic Tcell immunity. Science 2008, 322:1097-1100.
22. Honda K., Takeda K. Regulatory mechanisms of immune responses to intestinal bacteria. Mucosal Immunol. 2009, 2:187-196.
23. Hu W., Troutman T.D., Edukulla R., Pasare C. Priming microenvironments dictate cytokine requirements for T helper 17 cell lineage commitment. Immunity 2011, 35:1010-1022.
24. Ichikawa E., Hida S., Omatsu Y., Shimoyama S., Takahara K., Miyagawa S., Inaba K., Taki S. Defective development of splenic and epidermal CD4+ dendritic cells in mice deficient for IFN regulatory factor-2. Proc. Natl. Acad. Sci. USA 2004, 101:3909-3914.
25. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., Cua D.J., Littman D.R. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126:1121-1133.
26. Iwata M., Hirakiyama A., Eshima Y., Kagechika H., Kato C., Song S.Y. Retinoic acid imprints gut-homing specificity on Tcells. Immunity 2004, 21:527-538.
27. Jaensson E., Uronen-Hansson H., Pabst O., Eksteen B., Tian J., Coombes J.L., Berg P.L., Davidsson T., Powrie F., Johansson-Lindbom B., Agace W.W. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J.Exp. Med. 2008, 205:2139-2149.
28. Jaensson-Gyllenback E., Kotarsky K., Zapata F., Persson E.K., Gundersen T.E., Blomhoff R., Agace W.W. Bile retinoids imprint intestinal CD103+ dendritic cells with the ability to generate gut-tropic Tcells. Mucosal Immunol. 2011, 4:438-447.
29. Johansson-Lindbom B., Svensson M., Pabst O., Palmqvist C., Marquez G., Forster R., Agace W.W. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective Tcell homing. J.Exp. Med. 2005, 202:1063-1073.
30. Jongbloed S.L., Kassianos A.J., McDonald K.J., Clark G.J., Ju X., Angel C.E., Chen C.J., Dunbar P.R., Wadley R.B., Jeet V., et al. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J.Exp. Med. 2010, 207:1247-1260.
31. Jung S., Aliberti J., Graemmel P., Sunshine M.J., Kreutzberg G.W., Sher A., Littman D.R. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 2000, 20:4106-4114.
32. Kinnebrew M.A., Buffie C.G., Diehl G.E., Zenewicz L.A., Leiner I., Hohl T.M., Flavell R.A., Littman D.R., Pamer E.G. Interleukin 23 production by intestinal CD103(+)CD11b(+) dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense. Immunity 2012, 36:276-287.
33. Klein U., Casola S., Cattoretti G., Shen Q., Lia M., Mo T., Ludwig T., Rajewsky K., Dalla-Favera R. Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat. Immunol. 2006, 7:773-782.
34. Kobayashi T., Walsh P.T., Walsh M.C., Speirs K.M., Chiffoleau E., King C.G., Hancock W.W., Caamano J.H., Hunter C.A., Scott P., et al. TRAF6 is a critical factor for dendritic cell maturation and development. Immunity 2003, 19:353-363.
35. Kusunoki T., Sugai M., Katakai T., Omatsu Y., Iyoda T., Inaba K., Nakahata T., Shimizu A., Yokota Y. TH2 dominance and defective development of a CD8+ dendritic cell subset in Id2-deficient mice. J.Allergy Clin. Immunol. 2003, 111:136-142.
36. Langlet C., Tamoutounour S., Henri S., Luche H., Ardouin L., Gregoire C., Malissen B., Guilliams M. CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J.Immunol. 2012, 188:1751-1760.
37. Lewis K.L., Caton M.L., Bogunovic M., Greter M., Grajkowska L.T., Ng D., Klinakis A., Charo I.F., Jung S., Gommerman J.L., et al. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 2011, 35:780-791.
38. Mach N., Gillessen S., Wilson S.B., Sheehan C., Mihm M., Dranoff G. Differences in dendritic cells stimulated invivo by tumors engineered to secrete granulocyte-macrophage colony-stimulating factor or Flt3-ligand. Cancer Res. 2000, 60:3239-3246.
39. Mahida Y.R., Galvin A.M., Gray T., Makh S., McAlindon M.E., Sewell H.F., Podolsky D.K. Migration of human intestinal lamina propria lymphocytes, macrophages and eosinophils following the loss of surface epithelial cells. Clin. Exp. Immunol. 1997, 109:377-386.
40. Maloy K.J., Kullberg M.C. IL-23 and Th17 cytokines in intestinal homeostasis. Mucosal Immunol. 2008, 1:339-349.
41. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., Hatton R.D., Wahl S.M., Schoeb T.R., Weaver C.T. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006, 441:231-234.
42. Matozaki T., Murata Y., Okazawa H., Ohnishi H. Functions and molecular mechanisms of the CD47-SIRPalpha signalling pathway. Trends Cell Biol. 2009, 19:72-80.
43. Melton A.C., Bailey-Bucktrout S.L., Travis M.A., Fife B.T., Bluestone J.A., Sheppard D. Expression of alphavbeta8 integrin on dendritic cells regulates Th17 cell development and experimental autoimmune encephalomyelitis in mice. J.Clin. Invest. 2010, 120:4436-4444.
44. Meresse B., Ripoche J., Heyman M., Cerf-Bensussan N. Celiac disease: from oral tolerance to intestinal inflammation, autoimmunity and lymphomagenesis. Mucosal Immunol. 2009, 2:8-23.
45. Molenaar R., Greuter M., van der Marel A.P., Roozendaal R., Martin S.F., Edele F., Huehn J., Forster R., O'Toole T., Jansen W., et al. Lymph node stromal cells support dendritic cell-induced gut-homing of Tcells. J.Immunol. 2009, 183:6395-6402.
46. Mora J.R., Iwata M., Eksteen B., Song S.Y., Junt T., Senman B., Otipoby K.L., Yokota A., Takeuchi H., Ricciardi-Castagnoli P., et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 2006, 314:1157-1160.
47. O'Keeffe M., Hochrein H., Vremec D., Pooley J., Evans R., Woulfe S., Shortman K. Effects of administration of progenipoietin 1, Flt-3 ligand, granulocyte colony-stimulating factor, and pegylated granulocyte-macrophage colony-stimulating factor on dendritic cell subsets in mice. Blood 2002, 99:2122-2130.
48. Persson E.K., Jaensson E., Agace W.W. The diverse ontogeny and function of murine small intestinal dendritic cell/macrophage subsets. Immunobiology 2010, 215:692-697.
49. Poulin L.F., Salio M., Griessinger E., Anjos-Afonso F., Craciun L., Chen J.L., Keller A.M., Joffre O., Zelenay S., Nye E., et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J.Exp. Med. 2010, 207:1261-1271.
50. Poulin L.F., Reyal Y., Uronen-Hansson H., Schraml B.U., Sancho D., Murphy K.M., Hakansson U.K., Ferreira Moita L., Agace W.W., Bonnet D., Reis E.S.C. DNGR-1 is a specific and universal marker of mouse and human Batf3-dependent dendritic cells in lymphoid and nonlymphoid tissues. Blood 2012, 119:6052-6062.
51. Rivollier A., He J., Kole A., Valatas V., Kelsall B.L. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J.Exp. Med. 2012, 209:139-155.
52. Robbins S.H., Walzer T., Dembele D., Thibault C., Defays A., Bessou G., Xu H., Vivier E., Sellars M., Pierre P., et al. Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol. 2008, 9:R17.
53. Schiavoni G., Mattei F., Sestili P., Borghi P., Venditti M., Morse H.C., Belardelli F., Gabriele L. ICSBP is essential for the development of mouse type I interferon-producing cells and for the generation and activation of CD8alpha(+) dendritic cells. J.Exp. Med. 2002, 196:1415-1425.
54. Schulz O., Jaensson E., Persson E.K., Liu X., Worbs T., Agace W.W., Pabst O. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J.Exp. Med. 2009, 206:3101-3114.
55. Sciammas R., Shaffer A.L., Schatz J.H., Zhao H., Staudt L.M., Singh H. Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 2006, 25:225-236.
56. Scott C.L., Aumeunier A.M., Mowat A.M. Intestinal CD103+ dendritic cells: master regulators of tolerance?. Trends Immunol. 2011, 32:412-419.
57. Shaw M.H., Kamada N., Kim Y.G., Nunez G. Microbiota-induced IL-1beta, but not IL-6, is critical for the development of steady-state TH17 cells in the intestine. J.Exp. Med. 2012, 209:251-258.
58. Sun C.M., Hall J.A., Blank R.B., Bouladoux N., Oukka M., Mora J.R., Belkaid Y. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3T reg cells via retinoic acid. J.Exp. Med. 2007, 204:1775-1785.
59. Suzuki S., Honma K., Matsuyama T., Suzuki K., Toriyama K., Akitoyo I., Yamamoto K., Suematsu T., Nakamura M., Yui K., Kumatori A. Critical roles of interferon regulatory factor 4 in CD11bhighCD8alpha- dendritic cell development. Proc. Natl. Acad. Sci. USA 2004, 101:8981-8986.
60. Tamura T., Tailor P., Yamaoka K., Kong H.J., Tsujimura H., O'Shea J.J., Singh H., Ozato K. IFN regulatory factor-4 and -8 govern dendriticcell subset development and their functional diversity. J.Immunol. 2005, 174:2573-2581.
61. Thornton A.M., Korty P.E., Tran D.Q., Wohlfert E.A., Murray P.E., Belkaid Y., Shevach E.M. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J.Immunol. 2010, 184:3433-3441.
62. Uematsu S., Fujimoto K., Jang M.H., Yang B.G., Jung Y.J., Nishiyama M., Sato S., Tsujimura T., Yamamoto M., Yokota Y., et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 2008, 9:769-776.
63. Weiss J.M., Bilate A.M., Gobert M., Ding Y., Curotto de Lafaille M.A., Parkhurst C.N., Xiong H., Dolpady J., Frey A.B., Ruocco M.G., et al. Neuropilin 1 is expressed on thymus-derived natural regulatory Tcells, but not mucosa-generated induced Foxp3+ T reg cells. J.Exp. Med. 2012, 209:1723-1742. S1721.
64. Worbs T., Bode U., Yan S., Hoffmann M.W., Hintzen G., Bernhardt G., Forster R., Pabst O. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J.Exp. Med. 2006, 203:519-527.
65. Wu L., D'Amico A., Winkel K.D., Suter M., Lo D., Shortman K. RelB is essential for the development of myeloid-related CD8alpha- dendritic cells but not of lymphoid-related CD8alpha+ dendritic cells. Immunity 1998, 9:839-847.
66. Xavier R.J., Podolsky D.K. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007, 448:427-434.
67. Yadav M., Louvet C., Davini D., Gardner J.M., Martinez-Llordella M., Bailey-Bucktrout S., Anthony B.A., Sverdrup F.M., Head R., Kuster D.J., et al. Neuropilin-1 distinguishes natural and inducible regulatory Tcells among regulatory Tcell subsets invivo. J.Exp. Med. 2012, 209:1713-1722. S1711-1719.
68. Yokota A., Takeuchi H., Maeda N., Ohoka Y., Kato C., Song S.Y., Iwata M. GM-CSF and IL-4 synergistically trigger dendritic cells to acquire retinoic acid-producing capacity. Int. Immunol. 2009, 21:361-377.